Annals of Otology. Rhinology & Laryngology 120(11):7O7-7I2.

2011 Annals Publishing Company. All rights reserved.

Microbiology of Acute and Chronic Maxillary Sinusitis
in Smokers and Nonsmokers
Itzhak Brook, MD, MSc; Jeffrey N. Hausfeld, MD
Objectives: We evaluated the microbiology of sinus aspirates of smokers and nonsmokers with acute and chronic maxil-
lary sinusitis.
Methods: Cultures were obtained from 458 patients, 244 (87 smokers and 157 nonsmokers) of whom had acute maxil-
lary sinusitis and 214 (84 smokers and 130 nonsmokers) of whom had chronic maxillary sinusitis, between 2001 and
2007.
Results: A greater number of Staphylococcus aureus, methicillin-resistant 5 aureus (MRSA), and beta-lactamase-pro-
ducing bacteria (BLPB) were found in the 87 smokers with acute sinusitis than in the nonsmokers with acute sinusitis (p
< 0.005; p < 0.025, and p < 0.05, respectively). A greater number of these organisms were found in the 84 smokers with
chronic sinusitis than in the nonsmokers (p < 0.01, p < 0.025, and p < 0.001, respectively). Eighty-five BLPB isolates
were recovered from 73 patients (30%) with acute sinusitis. These included Moraxella catarrhalis, S aureus, Haemophi-
lus influenzae, Prevotella spp, and Fusobacterium spp; 40 BLPB isolates were found in smokers, and 45 in nonsmokers
{p < 0.05). One hundred twenty-five BLPB isolates were recovered from 91 patients (43%) with chronic sinusitis, includ-
ing M caarr/ia/, Bacteroides fragilis group, S aureus, H influenzae, Prevotella spp, and Fusobacterium spp; 69 BLPB
isolates were found in smokers, and 56 in nonsmokers (p < 0.001). Antimicrobial therapy had been administered in the
past month to 130 patients (28%; 60 smokers and 70 nonsmokers; p < 0.025). Both MRSA and BLPB were isolated more
often from these individuals (p < 0.025). However, the higher isolation rates of MRSA and BLPB in smokers were inde-
pendent of previous antimicrobial therapy.
Conclusions: These data illustrate a greater frequency of isolation of S aureus, MRSA, and BLPB in patients with acute
and chronic sinusitis who smoke.
Key Words: beta-lactamase, methicillin resistance, sinusitis, smoking, Staphylococcus aureus.
INTRODUCTION
Smoking has a significant impact on the oropha-
ryngeal bacterial fiora of children, as well as adults.'
Active smokers and those exposed to secondhand
smoke are at increased risk of bacterial infections
such as sinusitis,^ tuberculosis, pneumonia, and le-
gionnaires disease; bacterial vaginosis and sexually
transmitted diseases; Helicobacter pylori infection;
periodontitis; meningitis; otitis media; and postsur-
gical and nosocomial infections.^
No previous study has compared the microbiol-
ogy of sinus aspirates obtained from smokers to that
of those obtained from nonsmokers. This retrospec-
tive study evaluated the microbiology of sinus aspi-
rates of smokers and nonsmokers who had acute or
chronic maxillary sinusitis.
PATIENTS AND METHODS
The population studied was a middle-class one re-
siding in suburban locations in the vicinity of Wash-
ington, DC. The patients were consecutively seen in
the outpatient clinic between January 1, 2001, and
January 1, 2007, and had a diagnosis of acute or
chronic bacterial maxillary sinusitis.
The patients with acute infection had symptoms
that had lasted between 10 and 30 days, and those
with chronic infection had had symptoms for more
than 90 days. None of those with chronic sinusitis
had had previous sinus surgery. Smokers were de-
fined as individuals who had smoked at least 10 cig-
arettes a day for the past 5 years. The determination
was based on the patient's own history.
The patients' complaints included facial pain,
frontal headache, purulent nasal discharge, fever,
and malaise. Radiography with occipitomental (Wa-
ters view), lateral, oblique, and verticomental views
or computed tomography was performed. Sinus-
itis was defined radiographically as complete sinus
opacity, ie, an air-fluid level or mucous membrane
thickening of at least 6 mm in the maxillary sinus.
From the Department of Pediatrics, Georgetown University School of Medicine, Washington, DC.
Correspondence: Itzhak Brook, MD, MSc, 4431 Albemarle St NW, Washington, DC 20016.
707
708
Brook & Hausfeld, Smoking & Sinusitis
For the Waters view, mucosal thickening of the max-
illary sinuses was measured as the shortest distance
from the air-mucosal interface to the most lateral
part of the maxillary sinus wall. Specimens were ob-
tained through endoscopy, and the sinus secretions
were collected with calcium alginate-tipped micro-
swabs. The study was granted Institutional Review
Board approval.
Cultures were obtained endoscopically before
therapy with calcium alginate swabs that were imme-
diately plated into media supportive of the growth of
aerobic and anaerobic bacteria. The methods of spec-
imen collection, transportation, and microbiological
evaluation were previously described ."* Specimens
were processed semiquantitatively, and organisms
were identified by standard methods.^ Beta-lacta-
mase activity was determined by use of the chro-
mogenic cephalosporin analog 87/312 method.^
Staphylococcus qureus isolates were screened
for oxacillin resistance by the Clinical Laboratory
Standard Institute disk diffusion method.'' Over-
night cultures from blood agar plate were suspended
in Mueller-Hinton broth to the turbidity of 0.5 Mc-
Farland and plated on Mueller-Hinton agar, and a
l-^ig oxacillin disc was placed with the inoculum.
Zone diameters were measured and recorded after
a 24-hour incubation at 35C (susceptible, equal to
or less than 13 mm; intermediate, between 11 and
12 mm; and resistant, equal to or less than 10 mm).
Methicillin-resistant S aureus (MRSA) strains were
not typed.
All isolates of Streptococcus pneumoniae were
screened for penicillin susceptibility with a 1 -\ig ox-
acillin disk by the Kirby-Bauer disk diffusion meth-
od. Intermediate resistance to penicillin was defined
as a minimal inhibitory concentration of 0.1 to 1.0
|j,g/mL, and high resistance to penicillin was defined
as a minimal inhibitory concentration of at least 2.0
|a,g/mL.
Included in the final analysis were only patients
whose culture showed bacterial growth. Statistical
significance was calculated by Fisher's exact test
(2-sided) unadjusted.
RESULTS
,We evaluated 458 patients (244 with acute and
214 with chronic maxillary sinusitis) after exclusion
of an additional 110 patients (62 with acute and 48
with chronic sinusitis) whose culture did not show
any bacterial growth. The patients' ages ranged from
18 to 75 years (mean, 42 years 4 months); 265 were
male. No differences were noted in the age distribu-
tion, ethnicity, or gender of the patients.
TABLE 1. BACTERIOLOGY OF 244 PATIENTS WITH
ACUTE MAXILLARY SINUSITIS
Bacteria
Aer^obic bacteria
a-Hemolytic streptococci
Smokers
(N = 87)
4
Streptococcus pneumoniae 25
Intermediate resistance
to penicillin
High resistance to
penicillin
Group F streptococcus
Streptococcus pyogenes
Staphylococcus aureus
(methicillin-resistant)
Staphylococcus aureus
(methicillin-sensitive)
Staphylococcus
epidermidis
Haemophilus influenzae
Moraxella catarrhalis
Klebsiella pneumoniae
Pseudomonas aeruginosa
Proteus mirabilis
Fscherichia coli
Subtotal aerobes
Anaerobic bacteria
Peptostreptococcus spp
Veillonella prvula
Eubacterium spp
Propionibacterium acnes
Fusobacterium spp
7
3
2
4
8* (6)
7t(4)
4(2)
16(9)
15(15)
2
! 1
2
90 (36t)
6
2
1
2
1(1)
Fusobacterium nucleatum
Bacteroides spp
Prevotella
melaninogenica
Prevotella oralis
Prevotella oris-buccae
Prevotella intermedia
Porphyromonas
asaccharolytica
Subtotal anaerobes
Total
1(1)
2(1)
2(1)
1
18(4)
108 (40t)
Numbers within parentheses indicate
producing bacteria.
Nonsmokers
(N = 157)
9
54
8
4
4
7
4(3)
4(1)
4(1)
37(8)
29 (29)
1
1
1
1
156 (42)
15
2
3
2
2(1)
1
2(1)
2(1)
2
2
33(3)
189 (45)
Total
(N = 244)
13
79
15
7
6
11
12(9)
11(5)
8(3)
53(17)
44(44)
3
2
3
1
246 (78)
21
2
3
5
3(1)
2(1)
2(1)
4(2)
2(1)
2(1)
2
3
51(7)
297 (85)
number of beta-lactamase-
*Difference between smokers and nonsmokers, p < 0.025.
tDifference between smokers and nonsmokers, p < 0.05
Acute Sinusitis. Of the 244 patients, 87 were
smokers and 157 were nonsmokers. A total of 297
isolates were recovered (1.2 per specimen): 246 aer-
obic and facultative ( 1.0 per specimen) and 51 an-
aerobic (0.2 per specimen; Table 1). The number of
isolates varied from 1 to 3. Antimicrobial therapy
was administered to 45 patients (24%) in the month
before sample collection.
Aerobic and facultative organisms only were re-
Brook & Hausfeld, Smoking & Sinusitis
709
covered in 213 instances (87%), anaerobes only
were recovered in 15 (6%), and mixed aerobic and
anaerobic bacteria were recovered in 16 (7%). The
predominant aerobic bacteria were S pneumoniae
(79 isolates; 15 were intermediately resistant and 7
highly resistant to penicillin), Haemophilus influen-
zae (53), Moraxella catarrhalis (44), and S aureus
(23, including 12 that were methicillin-resistant; Ta-
ble 1).
The predominant anaerobes were gram-negative
bacilli (15 isolates, including 10 Prevotella, 3 Por-
phyromonas spp, and 2 Bacteroides spp), Pepto-
streptococcus spp (21), and Fusobacterium spp (5).
Eighty-five beta-lactamase-producing bacteria
(BLPB) were recovered from 73 patients (30%; Ta-
ble 1). These included all 44 M catarrhalis isolates,
14 of the 23 (61%) S aureus isolates, 17 of the 53
(32%) H influenzae isolates, 4 of the 10 (40%) Prev-
otella spp isolates, and 2 of th 5 (40%) Fusobacte-
rium spp isolates. Forty BLPB isolates were found
in smokers, and 45 in nonsmokers (p < 0.05).
A greater number of S aureus, MRSA, methi-
cillin-sensitive S aureus, and BLPB isolates were
found in smokers than in nonsmokers (p < 0.005, p
< 0.025, p < 0.05, and p < 0.05, respectively; Table
1). No other differences were noted in the recovery
of isolates between smokers and nonsmokers.
Chronic Sinusitis. Of the 214 patients, 84 were
smokers and 130 were nonsmokers. A total of 591
isolates were recovered (2.8 per specimen): 211 aer-
obic and facultative (1.0 per specimen) and 380 an-
aerobic (1.8 per specimen; Table 2). The number of
isolates varied from 1 to 5. Antimicrobial therapy
was administered to 85 patients (40%) in the month
before sample collection.
Aerobic and facultative organisms only were re-
covered in 42 instances (19%), anaerobes only in 59
(28%), and mixed aerobic and anaerobic bacteria
were recovered in 113 (52%). The predominant aer-
obic bacteria were S aureus (38 isolates, including
18 that were methicillin-resistant), microaerophilic
streptococci (22), M catarrhalis {16), H influenzae
(13), S pneumoniae (10 isolates, 3 of which were
intermediately resistant and 2 of which were high-
ly resistant to penicillin), Proteus mirabilis (12),
Pseudomonas aeruginosa (11), Klebsiella pneumo-
niae (10), and Escherichia coli (7; Table 2).
The predominant anaerobes were gram-negative
bacilli (157 isolates, including 100 Prevotella spp,
28 Porphyromonas asaccharolytica, and 15 Bacte-
roides fragilis group), Peptostreptococcus spp (118),
and Fusobacterium spp (57).
TABLE 2. BACTERIOLOGY OF 214 PATIENTS
WITH CHRONIC MAXILLARY SINUSITIS
Smokers Nonsmokers Total
Bacteria (N = 84) (N = 30} (N = 214)
Aerobic bacteria
a-Hemolytic streptococci 14
Microaerophilic 8
streptococci
Streptococcus pneumoniae 4
Intermediate resistance 2
to penicillin
High resistance to 1
penicillin
Group F streptococcus 2
Group G streptococcus 3
Streptococcus pyogenes 5
Staphylococcus aureus 13* (8)
(methicillin-resistant)
Staphylococcus aureus 11 (9)
(methicillin-sensitive)
Staphylococcus 4 (2)
epidermidis
Haemophilus influenzae 5 (3)
Moraxella catarrhalis 6 (6)
Klebsiella pneumoniae 5
Pseudomonas aeruginosa 4
Proteus mirabilis 5
Escherichia coli 3
Subtotal aerobes 93 (28*)
Anaerobic bacteria
Peptostreptococcus spp 44
Veillonella prvula 4
Eubacterium spp 3
Propionibacterium acnes 11
Fusobacterium spp 10 (4)
Fusobacterium nucleatum 15 (7)
Bacteroides spp 5(1)
Bacteroides fragilis group 5 (5)
Prevotella 13 (8)
melaninogenica
Prevotella oralis 1 (3)
Prevotella oris-buccae 11 (2)
Prevotella intermedia 10 (5)
Porphyromonas 12 (6)
asaccharolytica
Subtotal anaerobes 150(41) 230(35) 380(76)
Total 243(691) 348(56) 591(125)
Numbers within parentheses indicate number of beta-lactamase-
producing bacteria.
*Difference between smokers and nonsmokers, p < 0.025.
fDifference between smokers and nonsmokers, p < 0.001.
We recovered 125 BLPB isolates from 91 patients
(43%). These included all 16 M catarrhalis and 15
fragilis group isolates, 21 of the 38 (55%) S aureus
isolates, 9 of the 13 (69%) H influenzae isolates, 27
of the 100 (27%) Prevotella spp isolates, and 20 of
the 77 (29%) Fusobacterium spp isolates. Sixty-
21
14
6
1
1
7
4
7
5(1)
9(3)
4(1)
8(6)
10(10)
5
7
7
4
118(21)
74
11
6
13
12(4)
20(5)
9(3)
10(10)
15(3)
11(2)
13(2)
20(2)
16(4)
35
22
10
3
2
9
7
12
18(9)
20(12)
8(3)
13(9)
16(16)
10
11
12
7
211 (49)
118
15
9
24
22(8)
35(12)
14(4)
15(15)
28(11)
18(5)
24(4)
30(7)
28(10)
710 Brook & Hausfeld, Smoking & Sinusitis
nine BLPB isolates were found in smokers, and 56
in nonsmokers (p < 0.001).
A greater number of S aureus, MRSA, and BLPB
isolates were found in smokers than in nonsmokers
(p < 0.01, p < 0.025, and p < 0.001, respectively;
Tables 1 and 2). No other differences were noted in
the recovery of isolates between smokers and non-
smokers.
Effect of Previous Antimicrobial Therapy on Iso-
lation of MRSA and BLPB. Antimicrobial therapy
had been administered in the past month to 130 pa-
tients (28%; 60 smokers and 70 nonsmokers; p <
0.025). MRSA was isolated more often from pre-
viously treated individuals (14 of 130 patients, or
11%) than from those not previously treated (16 of
328, or 5%; p < 0.025); 10 of these 14 MRSA iso-
lates were from smokers, and 4 from nonsmokers (p
< 0.05). BLPB were also isolated more frequently
in those recently treated with antibiotics (58 of 130
patients, or 45%) than in those not treated (106 of
328, or 32%; p < 0.025); 34 of these 58 BLPB iso-
lates were from smokers, and 24 from nonsmok-
ers (p < 0.025). The antimicrobials administered to
the patients were amoxicillin (45 .instances), fiuo-
roquinolones (34), extended-spectrum macrolides
(21), amoxicillin-clavulanate (18), and cephalospo-
rins (12). The antimicrobials administered to the 14
patients in whom MRSA was isolated were fiuoro-
quinolones (8 instances), extended-spectrum mac-
rolides (5), and cephalosporins and amoxicillin-clav-
ulanate (1).
DISCUSSION
Our study confirms the predominance of S pneu-
moniae, H infiuenzae, M catarrhalis, group A be-
ta-hemolytic streptococci, and S aureus in commu-
nity-acquired acute sinusitis in adults.^ Similarly, S
aureus and anaerobic bacteria {Prevotella, Porphy-
romonas, Fusobacterium, and Peptostreptococcus
spp) were found to be the main isolates in chronic
sinusitis.^
Our data also illustrate that although similar or-
ganisms were recovered in acute and chronic sinus-
itis in smokers and nonsmokers, S aureus, MRSA,
and BLPB were more frequently recovered from
those who smoked. The higher isolation rates of
MRSA and BLPB in smokers were independent of
previous antimicrobial therapy.
We previously found a statistically significant
higher number of antibiotic-resistant organisms in
the sinuses of smokers who had acute sinusitis and
had undergone failed antimicrobial therapy, as com-
pared to their susceptibility before therapy, i'^ In con-
trast to our previous study,i*^ in which we compared
recovery of organisms in 20 patients with sinusitis
before therapy to that after therapy, in this study we
evaluated the isolation of organisms in smokers and
nonsmokers in a larger number of individuals. Even
though smokers often receive antimicrobial therapy
for respiratory infections, the higher rates of isola-
tion of MRSA and BLPB were independent of their
recent exposure to these antimicrobial agents.!'
Adults who smoke have an increased risk of re-
spiratory tract infections, including sinusitis,^''^ and
of oral colonization by potentially pathogenic bac-
teria.'^-''* These phenomena were explained by en-
hanced bacterial binding to epithelial cells of smok-
ers,'^ and by the low number of aerobic and anaero-
bic organisms with inhibitory activity against bac-
terial pathogens (interfering organisms) in the oral
cavity of smokers.'^''^ The high number of patho-
gens and the low number of interfering organisms
found in smokers revert to normal levels after com-
plete cessation of smoking.' Tobacco smoke also
compromises the antibacterial function of leuko-
cytes, including neutrophils, monocytes, T cells, and
B cells, providing a mechanistic explanation for in-
creased infection risk.'^ It is therefore not surprising
that smokers are more often exposed than nonsmok-
ers to antimicrobial therapies, which subsequently
lead to greater acquisition of antimicrobial resis-
tance, as was illustrated in our study.
The major BLPB recovered from our patients were
5 aureus, H infiuenzae, M catarrhalis, and Prevo-
tella, Porphyromonas, and Fusobacterium spp. The
recovery rate of aerobic and anaerobic BLPB in the
oropharynx has increased in recent years, and these
organisms were isolated in one study in more than
half of patients with head and neck infections, in-
cluding sinusitis.'^ BLPB can be involved directly
in the infection, protecting not only themselves from
the activity of penicillins, but also penicillin-suscep-
tible organisms. This protection can occur when the
enzyme beta-lactamase is secreted into the infect-
ed tissue or abscess fiuid in sufficient quantities to
break the penicillins' beta-lactam ring before it can
kill the susceptible bacteria.^o The actual activity of
the enzyme beta-lactamase and the phenomenon of
"shielding" have been demonstrated in fiuids from
acutely and chronically inflamed sinuses.^'
An increase in the recovery of MRSA was previ-
ously noted in various respiratory infections,^^ in-
cluding acute and chronic sinusitis,^-' as well as in
the nasal mucosa of normal individuals.^^ Smoking
was found to be a risk factor for nasal colonization
with MRS A.25
The presence of MRSA in the infected sinus may
Brook & Hausfeld, Smoking & Sinusitis
711
not only lead to failure of antimicrobial therapy, but
can also serve as a potential source for the spread
of these organisms to other body sites, as well as an
origin for dissemination to other individuals. Fur-
thermore, MRS A that also produces beta-lactamase
can survive treatment with beta-lactam antibiotics
and continue to protect penicillin-susceptible patho-
gens from penicillins.2"
The association between previous use of antimi-
crobial therapy and increased isolation of MRS A has
been noticed in community- and hospital-acquired
infections,^^2'' as well as in patients with sinusitis.^^
Like Gerencer,28 we found that the majority of pa-
tients with sinusitis infected with MRSA who were
previously treated with antimicrobials had been
treated with either a fluoroquinolone or an extend-
ed-spectrum macrolide antibiotic. Since almost all
strains of MRSA are resistant to these agents, it is
possible that these classes of antibiotics may be cre-
ating an environment within the sinuses that is par-
ticularly conducive to MRSA growth.
Treatment of sinus infection in smokers may
be more challenging than such treatment in non-
smokers. The higher rates of recovery of 5 aureus,
MRSA, and BLPB in these patients may require the
administration of antimicrobials effective against
these bacteria, as well as other potential aerobic
and anaerobic pathogens. Antimicrobials effective
against aerobic and anaerobic BLPB are amoxicillin
plus clavulanic acid, moxifloxacin, and the carba-
penems. Clindamycin is effective against anaerobic
BLPB, but has no activity against H influenzae.
Although vancomycin represents the gold stan-
dard of therapy for MRSA infections, reports of in-
creasing in vitro resistance to vancomycin ,^9 com-
bined with reports of clinical failures (with this and
other antistaphylococcal agents), underscore the
need for alternative therapies. Older agents with fa-
vorable in vitro activity available in both oral and
intravenous dose forms include trimethoprim-sul-
famethoxazole and clindamycin. Limited clinical
data exist to support their routine use as initial ther-
apy in the treatment of MRSA infections. However,
these and other options (eg, tetracyclines) are being
re-explored in the setting of increasing concern over
MRSA acquired in the community setting. Newer
treatment options for MRSA include linezolid, quin-
upristin-dalfopristin, daptomycin, and tigecycline.
Culture-directed oral and topical antibiotic therapy
has been effectively utilized in treatment of MRSA,
as well as BLPB-associated sinusitis.^^ Even though
the gold standard of obtaining such a culture is
through a surgical specimen or punctures ,3 cultures
obtained through meatal endoscopy have been re-
peatedly shown to provide adequate results.^' Topi-
cal application of antibiotics to the sinus membranes
offers the potential benefit of a high concentration
of the drug at the site of infection. Such topical an-
tibiotics include gentamicin, tobramycin, vancomy-
cin, ciprofloxacin, and mupirocin.
Further prospective studies and continuous moni-
toring of the rates of recovery of S aureus, MRSA,
and BLPB in smokers who present with acute and
chronic sinusitis are indicated. The results of our
study, which demonstrated the increased role of
MRSA and BLPB in sinusitis in smokers, under-
score the need to have a greater index of suspicion
for the presence of S aureus, MRSA, and BLPB in
smokers with sinusitis, and highlight the importance
of performing routine endoscopie cultures, especial-
ly in cases that fail to respond to empiric antimicro-
bial therapy.
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